The effects of exercise-based
interventions on repetitive autistic
behaviors
A Systematic Literature Review
Andreea Diana Ion
One year master thesis 15 credits Supervisor: Nerrolyn Ramstrand Interventions in Childhood
SCHOOL OF EDUCATION AND COMMUNICATION (HLK) Jönköping University
Master Thesis 15 credits Interventions in Childhood Spring Semester 2019
ABSTRACT
Author: Andreea Diana Ion
The effects of exercise-based interventions on repetitive autistic behaviors A Systematic Literature Review
Pages: 26
Repetitive behaviors are a core symptom of autism spectrum disorders. They represent a major barrier to learning and social adaptation, affect levels of engagement in life situations, communication, social interactions and sustain social connections. Repetitive behaviors are often managed using exercise-based interventions which have been suggested to reduce repetitive behaviors and benefit mental health and behavioral functioning of individuals with ASD. The purpose of this systematic review was to explore and critically review the findings of previous studies examining effects of various exercise-based interventions on reducing autistic repetitive behaviors in children with autism spectrum disorder. Searches were limited to peer-reviewed studies written in English and published between Jan.2008- Jan. 2019. Only studies focusing on physical exercise-based interventions aiming to decrease repetitive behaviors as a symptom of an autistic spectrum disorder were included. Quality of articles included in the review was assessed using the Joanna Briggs checklists. Two researchers were involved in the quality assessment process, and any discrepancies were resolved through discussion. 5 studies were included in the final review. All studies examined the effects of short term exercise interventions on repetitive behaviors in children with ASD. There was no consistency across studies regarding types or duration of interventions, sample sizes or demographics of participants. However, the findings of the studies examined in this review provide a moderate to strong evidence that exercise-based interventions decrease repetitive behaviors. The studies reviewed included clinically relevant findings that can be used and adapted to fit different needs of children in future interventions. However, additional research using stronger and more varied designs, would be needed to determine the most beneficial types of exercise- based interventions for decreasing repetitive behaviors.
Keywords: ASD; repetitive behaviors; exercise interventions; systematic review
Postal address Högskolan för lärande och kommunikation (HLK) Box 1026 551 11 JÖNKÖPING Street address Gjuterigatan 5 Telephone 036–101000 Fax 036162585
Table of Contents
1 Introduction ... 1
2 Aim and research question ... 4
3 Method ... 5
3.1 Search strategy ... 5
3.2 Inclusion and exclusion criteria ... 6
3.3 Extraction Protocol ... 8
3.4 Risk of bias (quality)assessment ... 8
3.5 Strategy of data synthesis ... 8
3.6 Ethical considerations ... 8 4 Results ... 9 4.1 Study characteristics ...11 4.2 Methodological quality ...15 4.3 Summary of evidence ...18 4.3.1 Interventions ...18 4.3.2 Repetitive behaviors ...19 5. Discussion ...22 5.1 Future research ...25 5.2 Clinical implications ...25 5.3 Limitations ...25 5.4 Conclusion ...26 6. References ...27
1
1 Introduction
Autism spectrum disorder (ASD) is a neurodevelopmental disorder that is increasing in prevalence, with four times more males than females affected (Werling & Geschwind, 2013). The global prevalence of autism is on the rise, with approximately 1 in 200 children being diagnosed with ASD. Autism is now recognized as the most common neurological condition affecting children and one of the most common developmental disabilities. Autistic spectrum disorders can include a variety of cognitive and neurobehavioral disorders represented by three major and distinctive attributes: impairments in socialization and lack of social skills, impairments in verbal and nonverbal communication and language development, and stereotypic and repetitive patterns of behaviors (Petrus, Adamson, Block, Einarson, Sharifnejad & Harris, 2008).
According to the diagnosis and statistical manual of mental disorder (American Psychiatric Association, 2013), the autism spectrum disorder comprise four separate disorders: autistic disorder, Asperger’s disorder, childhood disintegrative disorder and the pervasive developmental disorder. The diagnosis criteria for ASD include: inappropriate responses in conversations, misreading verbal interaction, difficulties in building friendships, dependency on routines, high sensitivity to changes in the environment, intense focus on inappropriate items. The symptoms may vary from mild to severe depending on each individual. Also, there are three core domains of ASD symptoms: reciprocal social interaction, restricted and repetitive pattern of behaviors and verbal and non-verbal communication. In order to diagnose, deficits in only two out of the three core domains are required: deficits in social interaction and restrictive and repetitive pattern of behavior (American Psychiatric Association, 2013).
Repetitive and stereotyped behaviors can include stereotyped use of language, rituals, repetition of movement, repetitive manipulation of objects, attachment to objects, aggressive or self-injurious behavior (Watt, Wetherby, Barber & Morgan, 2008).
Repetitive behaviors are a core symptom of autism spectrum disorders and they represent a major barrier to learning and social adaptation (Leekam, Prior & Uljarevic, 2011). According to the ICF-CY, we can describe repetitive behaviors as being activity limitations and participation restrictions. They are likely to hinder the child in focusing on and engage in life situations, prevent them from initiating communication, initiate or maintain social
2
interactions and sustain social connections, or to focus attention on specific activities (World Health Organization, 2001). Also, according to Bronfenbrenner’s system theory, the final outcome of the child is a sum of direct and indirect interactions between the child and all the systems (microsystem, mesosystem, exosystem, macrosystem and chronosystem) and therefore, by linking this theory to repetitive behaviors, we understand that it affects the child’s interactions with family members and peers (microsystem) and can as well influence the interactions between persons that are close to the child (mesosystem). It is also a major influence regarding the chronosystem, which is represented by environmental events and transitions that occur over the child's life and development (Bronfenbrenner & Evans, 2000).
Repetitive behaviors are classified into four subtypes according to the diagnosis and statistical manual of mental disorder IV: (a) preoccupation with restricted interests; (b) non-functional routines or rituals; (c) repetitive motor mannerisms (stereotypies); and (d) persistent preoccupation with parts of objects (American Psychiatric Association, 2013). Recent research has also proposed another subtype described as lower repetitive behaviors. This is considered to be characteristic of younger and lower functioning children. The majority of children with ASD present, at one point in their development, with one or more forms of repetitive behaviors, either involving movements made with their own body parts or actions performed using different objects (Leekam, Prior & Uljarevic, 2011).
Repetitive movements, such as rocking, hand flapping, spinning or twirling are self-stimulatory movements and they represent a manner for the child to calm himself. These movements usually occur when the senses are overstimulated by external factors such as bright lights, noises or smells. Self-harmful disruptive behaviors, such as biting oneself or banging their heads, can occur sometimes and are also included in this particular category (Autism Spectrum Disorders, 2018).
Repetitive speech patterns include echolalia, when a set of words or phrases are repeated over and over, or delayed echolalia, when words or phrases that were previously heard are repeated after a certain amount of time which can vary from minutes to months. Repetitive speech symptoms cause speech and language development to be delayed or to develop in a peculiar way (Autism Spectrum Disorders, 2018).
Common factors that trigger repetitive behaviors include stress, fear and anxiety. Causes may vary a lot depending on the individual and the context, but as an example we can pin-point a
3
sudden change in a routine, difficulties in expressing or communicating or perceiving the environment as unpredictable and chaotic (Autism Spectrum Disorders, 2018).
These maladaptive behaviors are typically dealt with using interventions of different types and varying intensities, including pharmacological and behavioral interventions (Bremer, Crozier & Lloyd 2016).
The main groups of medications that are used in the pharmacologic treatment of ASD are antipsychotics, serotonin reuptake inhibitors, and opioid antagonists. Previous research has shown a limited improvement in repetitive behaviors and related symptoms and, in some cases, adverse side effects.
Behavioral interventions aim to increase and improve social and behavioral skills by reducing repetitive behaviors. Another goal is to acquire a better regulation of arousal and anxiety condition through interventions that target these factors. Cognitive Behavioral Therapy is an effective method for treating and reducing anxiety in children with ASD. However, the extent to which it helps to decrease repetitive behaviors is unclear (Leekam, Prior & Uljarevic, 2011).
Another way of dealing with repetitive behaviors can be through exercise-based interventions. Since mental health state can be meliorated through physical activity in typically developed individuals, it has been suggested that exercise-based interventions may be useful in the treatment of ASD and repetitive behaviors and as well as benefiting mental health and behavioral functioning of individuals with ASD. It has also been argued that exercise-based therapies are much more cost-effective than traditional behavioral therapies, as they can be performed in a variety of settings and do not necessarily require a specific equipment set, as they are much more adaptable and flexible (Bremer, Crozier & Lloyd 2016). In addition to repetitive behaviors, children with ASD are often having difficulties with posture, coordination and fine motor skills in their early development (Petrus, 2008). Coordination represents the ability of an individual to use different parts of the body together, in a harmonious way with effective results (Dictionary, 2004). Fine motor skill, more commonly known as dexterity, represents the ability of an individual to coordinate small muscles and synchronize the movements of hands or fingers with the eyes (Dictionary, 2004).
Even though coordination and fine motor skill impairments are frequently observed and diagnosed in children with ASD, previous studies report inconsistent findings and these issues have generally received far less attention and interest compared to the well-known
4
communication and social interaction deficits. Recent neuroanatomical and neurophysiologic studies implicate cortical and subcortical areas as major contributors to impaired coordination and fine motor skills (Fournier, Hass, Naik, Lodha, & Cauraugh, 2010). Since these factors are related to physical characteristics and capacities they can be improved through physical exercise-based interventions. It has also been demonstrated that higher intensity exercise interventions are more effective than a lower intensity exercise in decreasing repetitive and disruptive behaviors (Petrus, 2008).
A preliminary scoping process was conducted and it has been found that there are very few studies looking at target exercise therapies or physiotherapeutic interventions in relation to repetitive autistic behaviors, rather than solely general exercises. Even though physical exercise has multiple benefits for all children, regardless of their well-being, a more complex developed routine, elaborated by a specialist may benefit children with ASD who present with repetitive behaviors.
For the purpose of this systematic review, exercise-based interventions were defined as any kind of routine organized and conducted by a specialist, teacher, or instructor, that involves physical exercise defined as the repetitive gross-motor movement requiring physical exertion (Lang, Koegel, Ashbaugh, Regester, Ence & Smith, 2010).
2 Aim and research question
The purpose of this systematic review is to explore and critically review the findings of previous studies examining effects of various exercise-based interventions on reducing autistic repetitive behaviors in children with autism spectrum disorder.
The research question being asked to guide this study is the following:
What evidence exists to support exercise-based interventions in decreasing repetitive behaviors in children with autistic spectrum disorder?
5
3 Method
This study was conducted in accordance with the PRISMA statement for reporting systematic reviews (Liberati et al, 2009) and the PRISMA checklist was used as a guide for accessing, identifying and reviewing relevant literature.
This review is a follow-up of an already existing systematic review (Petrus et al, 2008) which synthetized results from studies up until 2007. The present systematic review analyzed studies published between January 2008 to January 2019.
3.1 Search strategy
In order to identify relevant literature electronic databases were searched together with manually searching of reference lists in relevant articles.
The searching process began in February 2019, and it included the following databases: PubMed, CINAHL, Scopus, MEDLINE, PsycINFO, Web of Science. These databases were chosen because they were known to be relevant to health science domains and to containing a broad range of medical related literature.
The following search terms were consistently used across databases: physiotherapy, physical therapy, exercise, exercise therapy, exercise intervention, rehabilitation, ASD, autism, autistic, autism spectrum disorder, Asperger, stereotyped behavior, disruptive behavior, repetitive behavior. MeSh terms were also used in relevant databases.
6
Table 1. Search string
Search string
( (MM "Physical Therapy Modalities") OR AB ( physiotherapy or physical therapy ) OR TI ( physiotherapy or physical therapy ) OR AB exercise OR TI exercise OR AB exercise therapy OR TI exercise therapy OR AB exercise intervention OR TI exercise intervention OR AB rehabilitation OR TI rehabilitation ) AND ( (MM "Stereotyped Behavior") OR AB stereotyped behavior OR TI stereotyped behavior OR AB stereotypic behaviour OR TI stereotypic behaviour OR AB repetitive behavior OR TI repetitive behavior OR AB repetitive behaviour OR TI repetitive behaviour OR AB disruptive behavior OR TI disruptive behavior OR AB disruptive behaviour OR TI disruptive behavior ) AND ( ( (MM "Autism Spectrum Disorder") OR (MM "Autistic Disorder") ) OR AB ( asd or autism spectrum disorder or autism) OR TI ( asd or autism spectrum disorder or autism ) OR AB autis* OR TI autis* OR AB autistic OR TI autistic OR AB autism OR TI autism OR AB asperger OR TI Asperger AND ) Filters: peer review, English, research article, jan 2008-jan 2019
3.2 Inclusion and exclusion criteria
Searches were limited to peer-reviewed studies written in English, using human subjects and published between Jan.2008- Jan. 2019. The titles of studies identified in the initial search were screened and papers were excluded if they were exclusively related to medications, genetics, cognition, memory, communication or any other irrelevant topic. Afterwards, abstracts were reviewed to further determine their relevance for the study.
The following inclusion/ exclusion criteria were implemented to determine the final included studies (table 2):
7
Table 2. Inclusion and exclusion criteria
Inclusion Exclusion
Publication type
2008-2019
Studies published in English
Full text articles published in peer review journals and available as full texts
Participants
between 5-18 years of age
having a diagnosis of the autistic spectrum
having repetitive behavior as one of the symptoms
Intervention
Physical exercise-based intervention
Publication type
Theses, books, abstracts
Participants:
Newborns, infants, toddlers, adults
Studies not measuring/ looking at repetitive behaviors
Intervention
Studies focusing on interventions other than exercise-based
Study designs:
Quantitative and mixed-methods studies (case control studies, case series, cohort studies, randomize control trials
Study designs:
Qualitative studies
Case studies, case reports
Other systematic reviews
Studies in which exercise is used as a punishment (contingent exercise) do not represent the interest of this study because the notion or effect of punishment or the capacity of the physical act itself to serve as a punishment is not considered (by the author) an intervention which is appropriate for treating/ working with children. Therefore the studies in cause were not considered.
8
3.3 Extraction Protocol
A data extraction protocol was created in order to keep track of all the scientific sources used for conducting this literature review.
The following information was extracted from relevant articles: authors, title, year of publication, journal; aim of the study, research questions, study design, method, sample of participants, information regarding data collection, data analysis, results; discussion, limitations and conclusions.
3.4 Risk of bias (quality)assessment
All articles included in the final review were assed for quality using the appropriate Joanna Briggs checklists (Briggs, 2018). The articles were graded based on the appraisal questions provided considering the type of study design of the article. To answer the questions, a three symbols grading system was used, where the checkmark symbol was understood as “yes”, “X” as “no” and the question mark as “unclear” or “inapplicable”. The legend of symbols is also provided and can be observed in the quality assessment tables provided in the methodological quality section, under results.
The quality criteria for articles to be included were that an article could not have more than two negative or unclear points accumulated. For case series studies, the articles that were graded with a score of less than 8 points out of 10 in the Joanna Brigs quality assessment checklist were excluded. For case control studies, the articles that were graded with a score of less than 8 points out of 10 were excluded. For randomize controlled trial studies, the articles that were graded with a score of less than 11 points out of 13 were excluded. Two researchers were involved in the quality assessment process, and any discrepancies were resolved through discussion. When there was no possibility of coming to a common conclusion about the quality of an article or about including or excluding it, the article in question was excluded.
3.5 Strategy of data synthesis
Data was synthesized according to the type of intervention and manifestation of repetitive behaviors presented in the study.
3.6 Ethical considerations
Several ethical considerations must be taken into account when conducting research, especially when the topic involves vulnerable groups such as children with special needs, as it
9
is the case in this present systematic review. The main overall goal of all the studies included in this paper was to improve the development and overall quality of life of the participants involved in the interventions and to bring new and relevant findings to the already existing literature. All studies followed the primum non nocere principle and the interventions processes were first of all in accordance to the human rights and for the benefit of all persons involved (Jahn, 2011). All the articles included specifically mentioned that they had received prior parental consent. Furthermore, two of the studies (Srinivasan et al., 2015 and Bahrami et al., 2012) also reported that the ethics committee assessed their protocol and provided an ethical approval, while the other three articles did not mention this detail. Also, all of the articles mentioned that any personal data or information regarding the participants was not disclosed and pseudonyms were used when appropriate.
4 Results
The initial database search resulted in 108 articles being identified from databases and an additional 25 articles through manual searching and reference searching. A total of 133 articles were screened(titles and abstracts) for eligibility, 79 articles did not meet the inclusion criteria and were removed. In addition, 23 duplicates were identified and removed. The remaining 31 articles were read in full text and 20 were excluded as following: 13 for not having the appropriate designs: systematic reviews, thesis, commentaries, study protocols; 3 because the participants’ age did not fit the inclusion criteria: newborns, infants or adults; 2 for not being intervention studies; 1 for being published before 2008; and 1 for not measuring repetitive behaviors.
The remaining 11 articles underwent critical appraisal using the Joanna Briggs critical appraisal checklists: (Tse, Pang & Lee, 2018; Neely, Rispoli, Gerow & Ninci, 2015; Losinski, Cook, Hirsch & Sanders, 2017; Schmitz, Mcfadden, Golem, Pellegrino, Walker, Sanders & Arent, 2017; Jiménez Martínez, Santana Rodríguez, Mateos Padorno & Montesdeoca Hernández, 2018; Srinivasan, Park, Neelly & Bhat, 2015; Operto, Martino, Rinaldi, Cerracchio, Salvati, Orza... & Farello, 2017; Anderson-Hanley, Tureck & Schneiderman, 2011; Casellato, Gandolla, Crippa & Pedrocchi, 2017; Bahrami, Movahedi, Marandi & Abedi, 2012; Chan, Sze, Siu, Lau & Cheung, 2013). 6 articles were removed due to poor methodological qualiy. A total of 5 articles were finally included in this review.
10
Table 3. Flow chart of the searching procedure.
No. of records identified through database searching: 108
No. of records identified through other sources: 25
No. of duplicates removed: 23 No. of records reviewed on title
and abstract level: 133
No. of records removed based on title and abstract: 79
No. of full text articles assessed for eligibility: 31
No. of full text articles excluded after quality assessment: 6
Final no of articles included: 5
No. of articles excluded after full text screening: 20
13 for not having the appropriate designs 3 for the reason that the participants’ age did not fit the inclusion criteria
2 for not being intervention studies 1 for being published before 2008 1 for not measuring repetitive behaviors
11
4.1 Study characteristics
A total of 5 articles, published from 2011-2015, involving a total number of 126 subjects were included as scientifically admissible for this systematic review: Neely, Rispoli, Gerow & Ninci, 2015; Srinivasan, Park, Neelly & Bhat, 2015; Anderson-Hanley, Tureck & Schneiderman, 2011; Bahrami, Movahedi, Marandi & Abedi, 2012; Chan, Sze, Siu, Lau & Cheung, 2013. The study designs included 3 case series studies, 1 case control study and 1 randomized controlled trial. All participants were children with ages between 5-18 years old, with males representing of 86.5% of participants. All participants were diagnosed with ASD, recruited through autism institutes and clinics, primary and secondary schools or fliers and online advertisings. They represented with repetitive behaviors which manifested as repetitive language, self-injurious behaviors and motor stereotypies: repetitive rocking and repetitive bouncing, repetitive arm swinging and repetitive head touching, and impulsive behaviors. No study measured or described any other additional secondary impairment. The interventions investigated included: jumping on an indoor trampoline, rhythm and robotic therapies, dance and cyber cycling, kata training, Chinese based mind-body exercise Nei Yang Gong and Progressive Muscle Relaxation technique. The period of time during which the interventions were applied varied from 2-14 weeks.
12
Table 4. Study identification
Title Authors Year
published Study design Effects of Antecedent Exercise on
Academic Engagement and Stereotypy During Instruction
Leslie Neely, Mandy Rispoli, Stephanie Gerow and Jennifer Ninci
2015 case series
A comparison of the effects of rhythm and robotic interventions on
repetitive behaviors and affective states of children with Autism
Spectrum Disorder (ASD)
Sudha M. Srinivasana, Isabel K. Parkc, Linda B. Neellyd, and Anjana N. Bhata
2015 case series
Autism and exergaming: effects on repetitive
behaviors and cognition
Cay Anderson-Hanley Kimberly Tureck Robyn L Schneiderman
2011 case series
Kata techniques training consistently decreases stereotypy in
children
with autism spectrum disorder
Fatimah
Bahrami,Ahmadreza Movahedi, Sayed Mohammad Marandi, Ahmad Abedi
2012 case control study
A Chinese Mind-Body Exercise Improves Self-Control of Children with Autism: A Randomized Controlled Trial
Agnes S. Chan, Sophia L. Szel, Nicolson Y. Siu, Eliza M. Lau, Mei-chun Cheung
2013 Randomized controlled Trial study
13
Table 5. Participants
Authors Participants age, gender Sample size Recruitment
Neely et al., 2015 1 male- 7 years old and 1 female- 8
years old 2
university-supported autism clinic
Srinivasan et al.,2015 32 males and 4 females between 5
and 12 years 36
through fliers posted online and onsite in local schools, services
Anderson-Hanley et al., 2011
8 male 4 female (mean age = 14.8 years +
10 participants, all males (mean age 12+10
recruited through a letter sent to parents
by a school administrator and announcements sent to ASD organizations
Bahrami et al., 2012
30 children with ASD (26 males and 4 females) ranging in age from 5 to
16 years (M = 9.13 years)
30
randomly selected from 200 students attending the autism
institute.
Chan et al., 2013 46 children, aged between 6 and 17 46
three primary schools and one secondary school in Hong Kong
using an online advertisement and application platform
14
Table 6. Diagnosis
Diagnosis Repetitive disruptive behaviors
Authors Defined
as Measured- how? Symptoms Manifestation
Neely et al.,
2015 ASD
Gilliam Autism Rating Scale–2 and Autism Spectrum Rating Scale
Motor rep behaviors
repetitive rocking and repetitive bouncing, repetitive arm swinging and
repetitive head touching
Srinivasan et
al.,2015 ASD Repetitive Behavior Scale – Revised (RBS-R)
repetitive behaviors
self-injurious behaviors, repetitive language
Anderson-Hanley et al.,
2011
ASD Gilliam Autism Rating Scale, 2nd edition
repetitive
behaviors unspecified
Bahrami et al.,
2012 ASD
Gilliam Autism Rating Scale, 2nd edition
repetitive
behaviors unspecified
Chan et al.,
2013 ASD
Gilliam Autism Rating Scale, 2nd edition
Repetitive behaviors
Impulsive self injurious behavior, Obsessive behavior repetitive language
15
Table 7. Intervention
Authors Type of intervention Frequency and duration
of intervention Comparison group
Neely et al., 2015 jumping on an indoor trampoline
2-3 days/ week, 10 minutes long,
10-12 weeks long
none
Srinivasan et al.,2015 rhythm and robotic therapies 4 sessions/ week 8 weeks long
Control, robot and rhythmic
Anderson-Hanley et al.,
2011 exergaming and cybercyckling
1sesion/ week, 30 mins long, 2 weeks long
Pilot I-Dance(exergaming)
and Pilot II-cybercycling
Bahrami et al., 2012 kata training 4 sessions/ week. 14 weeks long
15 participants assigned to an exercise and 15 assigned to a no-exercise control group
Chan et al., 2013
Chinese Chan-based mind-body exercise, Nei Yang Gong(experimental group), and Progressive Muscle Relaxation (PMR) technique (control group) 2 sessions/ week, 4 weeks long Experimental group (Chinese mind-body)
and control group (PMR)
4.2 Methodological quality
Neely et al., 2015 and Srinivasan et al., 2015 scored 9 points out of 10, being graded negatively for lacking details of the participants demographics, respectively clinic demographics. Clinic demographic details, as well as participant’s demographic details were not available in the most part of the articles analyzed. Anderson-Hanley et al., 2011, scored 8 points out of 10, being graded negatively for both clinical and participants’ demographics details. The quality assessment criteria and grading is presented in table 8.
16
Table 8. Case series quality assessment and grading
Bahrami et al., 2012 scored 8 points out of 10, being graded negatively for not identifying confounding factors (baseline characteristics, prognostic factors, or concomitant exposures) and strategies to deal with this. As defined in the Joanna Briggs checklist for case control studies, confounders represent differences between the comparison groups and they can influence the study results. Strategies to deal with effects of confounding factors may be handled by matching or stratifying samples of participants or by assessing the statistics used in the study (Briggs, 2018). The quality assessment criteria and grading is presented in table
9. Case series Yes ❌ No ? Unclear Neely et al., 2015 Srinivasan et al., 2015 Anderson-Hanley et al., 2011
1. Were there clear criteria for inclusion in the case series? 2. Was the condition measured in a standard, reliable way for all
participants included in the case series?
3. Were valid methods used for identification of the condition for all participants included in the case series?
4. Did the case series have consecutive inclusion of participants? 5. Did the case series have complete inclusion of participants? 6. Was there clear reporting of the demographics of the participants in the
study?
❌
7. Was there clear reporting of clinical information of the participants? ❌ 8. Were the outcomes or follow up results of cases clearly reported? 9. Was there clear reporting of the presenting site(s)/clinic(s)
demographic information?
❌ ❌
17
Table 9. Case control quality assessment and grading
Case control Yes ❌ No ? Unclear Bahrami et al., 2012
1. Were the groups comparable other than the presence of disease in cases or the absence of disease in controls?
2. Were cases and controls matched appropriately? 3. Were the same criteria used for identification of cases and controls? 4. Was exposure measured in a standard, valid and reliable way? 5. Was exposure measured in the same way for cases and controls?
6. Were confounding factors identified? ❌
7. Were strategies to deal with confounding factors stated? ❌ 8. Were outcomes assessed in a standard, valid and reliable way for cases and controls? 9. Was the exposure period of interest long enough to be meaningful? 10. Was appropriate statistical analysis used?
Chan et al., 2013 scored 11 points out of 13, being graded unclear for participants being blind to treatment assignment and for the trial design being appropriate, as these factors were not discussed within the study.
Blinding refers to the fact that participants should not be aware about which group they had been allocated to, as this may increase the risk of them behaving differently towards the intervention process and may compromise the results of the study (Briggs, 2018). The quality assessment criteria and grading is presented in table 10.
18
Table 10. Randomized controlled trial quality assessment and grading
4.3 Summary of evidence 4.3.1 Interventions
The exercise-based interventions examined in the 5 studies are varied and not many similarities can be found between them. However, 3 of them focused on rhythmic physical exercise: physical exercise conducted prior to instructional sessions (antecedent physical exercise) consisting of jumping on a trampoline located indoors in a therapy room (Neely et al., 2015); rhythmic movement-based activities (dance, yoga), robotic intervention (robot-child interactions) and play therapies (building blocks and art and crafts) which focused on group synchrony (Srinivasan et al., 2015); and exergaming intervention consisted of a
dance-Randomized controlled Trial
Yes ❌ No
? Unclear
Chan, Sze, Siu, Lau & Cheung,
2013
1. Was true randomization used for assignment of participants to treatment groups?
2. Was allocation to treatment groups concealed?
3. Were treatment groups similar at the baseline?
4. Were participants blind to treatment assignment? ?
5. Were those delivering treatment blind to treatment assignment?
6. Were outcomes assessors blind to treatment assignment?
7. Were treatment groups treated identically other than the intervention of interest? 8. Was follow up complete and if not, were differences between groups in terms of their follow up adequately
described and analyzed?
9. Were participants analyzed in the groups to which they were randomized?
10. Were outcomes measured in the same way for treatment groups?
11. Were outcomes measured in a reliable way?
12. Was appropriate statistical analysis used?
13. Was the trial design appropriate, and any deviations from the standard RCT design (individual randomization,
19
based intervention and sessions of cyber-cycling (Anderson-Hanley et al., 2011). The premise for implementing rhythm interventions, as stated by Srinivasan et al., 2015 is that children with ASD enjoy and have better abilities to perceive music. The interventions focused on motor skills as balance, coordination and dexterity.
Bahrami et al., 2012 examined the effects of kata training on repetitive behaviors. Kata represents a pattern of movements belonging to the martial arts made to be practiced alone or within groups. Kata sessions were taught by certified trainers. Intervention consisted of teaching strategies (fractionation, simplification and segmentation), verbal instructions, physical and manual guidance . The sessions were held in an indoor sports hall. The duration of sessions were increased from 30 minutes to 90 minutes over the course of the first 8 weeks.
Chan et al., 2013 aimed to compare the effect of a traditional Chinese Chan-based mind-body exercise, comprising movements like: tranquil stand, shoulder relaxation, nasal bridge massage, Qi-circulating movement, and passive Dan Tian breathing and promoting self-awareness and self-control with a Chinese adaptation of the Progressive Muscle Relaxation (PMR) based on sequentially tensing and relaxing seven muscle groups (nose, mouth, shoulders, arms, hands, chest and feet).
4.3.2 Repetitive behaviors
Neely et al., 2015 reported the repetitive behaviors being manifested as motor stereotypy (repetitive rocking and repetitive bouncing, repetitive arm swinging and repetitive head touching). Participants GARS-2 reported scores were 111 for the female participant and 97 for the male participant prior to the intervention. Both participants showed a decrease level of stereotypy during the exercise session that followed the actual intervention represented as a brief antecedent physical exercise. The female participant had a 66% mean stereotypy level prior to the antecedent exercise intervention, which decreased to 34% following the antecedent exercise. For the male participant, the prior mean stereotypy level was 28%, decreasing to 12% following the intervention. However, the antecedent exercise sessions that reached a behavioral satiation condition produced a higher than the baseline level of motor repetition for both participants. The time until satiation for the male participant was 6 min. 18 s. while for the female participant was 9 min. 37 s.
Two of the studies (Srinivasan et al., 2015 and Chan et al., 2013) reported the
repetitive behaviors being manifested as echolalia (repetitive use of language), impulsive and self-injurious behavior. Both of the studies reported no significant decrease in the repetitive
20
language after the intervention, as this component did not represent the target of any of the interventions. Srinivasan et al., 2015 measured the mean severity level of self-injurious behaviors in the early and late session of the intervention and reported that rhythmic movement-based activities (rhythm, dance, yoga) lead to a reduction in self-injurious behaviors (early session M=22.6 and late sessions M=15.4 ). In contrast, the robotic
intervention (robot-child interactions) did not demonstrate any behavioral improvements due to the technical limitations of the robot that made the context less appealing and causing some negative behaviors including tantrums and boredom (early session M=17.9 and late sessions M=22.1). The comparison group showed no behavioral improvement due to the sedentary context of the activities (early session M=8.8 and late sessions M=9.6).
Chan et al., 2013 reported that both the control (PMR) and the experimental (Chinese mind-based) groups showed a decrease in impulsive behaviors. However, following the mind-body intervention more noticeable improvement in self-control was observed (pre-intervention M=5.51 and post-intervention M=4.91), compared with the control group (pre-int. M=5.37 and post-int. M=5.28). A decrease in impulsive behaviors was as well observed for the experimental group (pre-int. M=7.78 and post-int. M=6.29). Chan et al., 2013 also looked at obsessive behaviors and reported only a slightly significant difference between the
experimental and the control group after the intervention.
Anderson-Hanley et al., 2011 and Bahrami et al., 2012 did not report on how the repetitive behaviors were manifested, but both studies used the GARS-2 scale to measure the behaviors. Anderson-Hanley et al., 2011 recorded the participants while playing for 5 minutes both before and after the intervention and used the recordings to code the repetitive behaviors. Also, both studies found no significant difference between the behaviors of the participant prior to the intervention. Bahrami et al., 2012 found a significant decrease in repetitive behaviors in the intervention group, as the mean stereotypy severity scores decreased from the pre-intervention time (M = 12.53 _ 6.92) to post-intervention time (7.20 _ 5.65) by an average of 5.33 points. No significant difference was observed for the control group, as the mean stereotypy severity scores decreased from the pre-intervention time (M = 14.47 _ 7.71) to post-intervention time (M = 13.93 _ 8.55) by an average of 0.53 points. However, it is also reported that the mean stereotypy severity scores increased from the post-intervention measurement until the follow-up measurement (1 month later) by an average of 0.87 points. No significant difference was found for the control group.
21
Anderson-Hanley et al., 2011 reported that for the first pilot group (exergaming) the average GARS-2 score was 70.7 and for the second pilot group (cybercycling) the average GARS-2 score was 78.8. A decrease in repetitive behaviors in participants involved in both of the pilot groups after the interventions), compared with their baseline condition was noticed but, repetitive behaviors decreased significantly after cybercycling( the mean M of repetitive behaviors pre-intervention was M= 9.7 and post intervention M=8.6), while after exergaming an improvement was shown only compared to the baseline condition( pre-intervention M=14.9 and post-intervention M=10.8).
Due to the inconsistency across the interventions implemented by the studies, themes could not emerge from the data and therefore the results were mainly reported separately. The results are presented below in table 11.
Table 11. Results
Study Analysis Result
Neely et al., 2015 observation of repetitive behaviors- % of mean stereotypy level in 10 sec. intervals
Female participant pre 66% / post 34%
Male participant pre 28% / post 12%
Chan et al., 2013 ANOVA- mean stereotypy level
Control group Self-control Pre M=5.37 / Post M=5.28 Impulsive behaviors Pre M=9.46 / post M= 11.89
Experimental group Self-control Pre M=5.51 / Post M= 4.91 impulsive behaviors Pre M=7.78 / post M=6.29
Bahrami et al., 2012 T test between groups Control group Pre M = 14.47 _ 7.71 Post M = 13.93 _ 8.55 Follow-up M=13.40 _ 7.66
Exercise group Pre M = 12.53 _ 6.92 Post M= 7.20 _ 5.65 Follow-up M= 8.07 _ 5.82
Srinivasan et al., 2015
ANOVA- mean stereotypy level
Rhythmic early M=22.6 / late M=15.4
Robotic early M=17.9 / late M=22.1
Control early M= 8.8/ late M=9.6 Anderson-Hanley et
al., 2011
ANOVA- mean stereotypy level
Cybercycling pre M=9.7 / post M= 8.6
22
5.
Discussion
This systematic review aimed to explore and review evidence related to the effects of exercise-based interventions on reducing repetitive behaviors in children with ASD. It has been suggested that exercise interventions have an important role in the treatment of children with ASD and in an earlier systematic review analyzing studies published between 1980 and 2007 it was suggested that exercise interventions are beneficial in managing repetitive behaviors. Following- on from the previous published review (Petrus et al., 2008), the present review explored literature from 2008 until 2019 to determine if any new evidence has been generated to support use of exercise-based interventions in decreasing repetitive behaviors in children with ASD. 5 new studies were identified and results support the previous review in providing evidence that exercise therapy is beneficial. However, the specific types of therapies identified in the present review differed from the previous work and it is difficult to make specific recommendations regarding the most appropriate type of therapy to manage repetitive behaviors.
The sample of participants across the 5 studies included in this review included a total of 126 subjects (with an average of 27.2 participants per study), with an age range from 5 to 18 years. In the previous systematic review (Petrus et al., 2008), the total number of participants across all 7 studies analyzed was 26 (with an average of 3.2 participants per study), with an age range of 4 to 15 years. Age and characteristics of participants varied across studies included in both this systematic review and the previous one (Petrus et al., 2008). The sample of participants across the studies included in this paper was considerably larger.
In this systematic review, repetitive behaviors in participants were measured using Gilliam Autism Rating Scale, 2nd edition and the Repetitive Behavior Scale – Revised (RBS-R). In Petrus et al., 6 of the studies (one study did not include this detail) measured repetitive behaviors using time-sampling techniques based on observation regarding the occurrence or non-occurrence of behaviors at specific time points.
None of the studies analyzed in this review described the parameters or intensity (aerobic/ anaerobic) of the exercise, even though previous research, as mentioned in Petrus et al, indicated that high-intensity exercises tend to be more efficient in decreasing repetitive
23
behaviors (Kern et al., 1984). It is important that future research addresses this issue so that recommendations regarding the most efficient type of exercises can be provided to therapists.
All 5 studies included in this review examined the effects of short term exercise interventions on repetitive behaviors in children with ASD. 3 studies based their interventions on rhythmic physical exercise (Neely et al., 2015; Srinivasan et al., 2015; Anderson-Hanley et al., 2011 ), while the other 2 promoted discipline, self-awareness and self-control (Bahrami et al., 2012; Chan et al., 2013). No two studies utilized the same intervention. Rhythmic
interventions were efficient in decreasing self-injurious behaviors and motor stereotypies. According to Srinivasan et al., the enjoyable nature of rhythmic interventions created positive experiences for children and induce positive states and emotions, which leads to a reduction of self-injurious behaviors (Srinivasan et al., 2015). Self-awareness and self-control
interventions also lead to significant decrease in impulsive behaviors and an improvement in self-control. According to Chan et al., the effectiveness of self-awareness and self-control exercises (martial arts) are related to the emphasis on discipline and character development, which tends to relieve anger and distress and automatically decreases impulsive behaviors (Chan et al., 2013). Repetitive use of language was managed using rhythmic and self-awareness interventions but no significant decrease was observed. In addition, obsessive behaviors showed no significant decreased following the self-awareness based intervention (Chan et al., 2013). One study (Bahrami et al., 2012) implementing a discipline and self-control based intervention reported that repetitive behaviors showed a significant decrease right after the intervention, but then they increased until the follow-up time check.
In comparison, the Petrus et al. review indicated that the consistency between interventions was high, as six of the seven studies analyzed used jogging as an intervention. However, when comparing the results of the two systematic reviews, we can conclude that they are very similar: a decrease in repetitive behaviors was reported in all of the studies analyzed by Petrus et al., as well as in this systematic review. Moreover, studies analyzed by both reviews reported that the post-intervention effects upon repetitive behaviors varied in duration, but none of them were maintained over a long period of time and the decrease of repetitive behaviors was temporary and dependent on the duration of the intervention.
The similarities in results as well as the short term effects upon repetitive behaviors, contrast with the fact that the sample and type of intervention vary a lot across the two systematic reviews. A reason for the short term effects might be the fact that the time duration
24
of all of the interventions (both systematic reviews) was limited and none of them were implemented as a periodical treatment. Therefore, the short term positive effects might not necessarily be related to the type of intervention used, but to the limited period of intervention.
It is important that clinicians are aware of these research findings whenever they are prescribing any form of treatment, as in some cases, exercise-based interventions can supersede medication (Petrus et al., 2008). Additional sources of previous research also confirmed positive influence of physical exercise on repetitive behaviors in children with ASD (Bremer et al., 2016) and evidence was found that physical exercise should be matched with stereotypic behavior in children with ASD (Tse, Pang & Lee, 2018). Also, as a secondary outcome following exercise-based intervention, an overall improvement with regard to social and adaptive abilities was observed in a large number of subjects (Operto et al., 2017) as well as increasing cognitive control (Anderson-Hanley et al., 2011) and attentional flexibility (Mostert-Kerckhoffs, Staal, Houben & de Jonge, 2015). Most importantly, physical activity in general, is known to positively influence the overall quality of life of all individuals, which means that its practice on children with ASD is essential and beneficial in areas beyond that investigated in the present review (Jiménez Martínez, Santana Rodríguez, Mateos Padorno & Montesdeoca Hernández, 2018).
Furthermore, reporting the findings of the analysed studies to the systems theory framework described in the background section, considering the fact that the interventions had mostly positive results regarding the various manifestations of repetitive behaviors, we can conclude that the overall well-being of the children increased. Also, by decreasing repetitive behaviors (which as mentioned before, represent a barrier in the children’s social life and a major risk factor for their final outcome) the quality of interactions between the children and different systems is most likely to be improved and a more beneficial environment for the children and all the other parties involved into their upbringing is created. Lastly, it can as well be assumed that the overall development of the children benefit from the decrease of repetitive behaviors and a higher rate of developmental progress will follow as a natural consequence (Bronfenbrenner & Evans, 2000).
25
5.1 Future research
Additional research using longitudinal designs with higher level of evidence (randomized control trials) and improved statistical power would be needed to determine the appropriate and most beneficial types of exercise-based interventions for decreasing repetitive behaviors. Interventions conducted for longer periods of time would probably be necessary in order to obtain more sustainable effects. Also, no study analyzed measured or reported any additional impairment in participants.
5.2 Clinical implications
While this review presents evidence that exercise-based therapy facilitates reduction of repetitive behaviors, no specific type of exercise intervention can be recommended. As such it is recommended that the intervention be adapted and tailored to the individual and their specific characteristics needs and tolerance levels in order for the process to have the higher efficiency and the child to be able to reach his maximum potential.
Exercise-based or physiotherapeutic interventions can address physical affections (obesity, scoliosis, fine coordination, balance, and so on) in parallel with the neurodevelopmental disorder, and physical exercises can be adapted to work towards alleviating multiple affections. Specific physiotherapeutic interventions (therapies) implemented by professionals and based on several goals, where decreasing repetitive behaviors would represent the main goal and additional impairments would be targeted as secondary goals should be conducted in order to improve children’s quality of life on a broader spectrum. Following the same target, a more holistic, interdisciplinary, child-centered approach including collaboration between family and professionals from various fields would provide a broader perspective upon the development of the treatment process and a better quality of the intervention (Björck-Åkesson, 2019).
5.3 Limitations
Articles included in this systematic review were limited to English, and therefore evidence from sources published in any other languages is lacking. Studies published prior to 2008 were excluded for the reason that another systematic review focusing on the same variables was conducted and analyzed studies between 1980 and 2007. Only peer-reviewed, published articles were included and therefore other relevant data from additional sources may be missing. Even though the quality appraisal was conducted by two different
26
researchers, the search process was conducted by a single person, so it is possible that some relevant articles or databases were missed.
5.4 Conclusion
The evidence of studies analyzed in this systematic review is moderate to strong, so we can conclude that exercise-based interventions decrease the repetitive behaviors in children with ASD. From all the exercise-based interventions included in the studies analyzed, we can conclude that interventions based on rhythmic physical activities (jumping, cycling, dancing, yoga) were the most common and efficient approach towards decreasing repetitive behaviors in children with ASD. Physiotherapists, clinicians and other specialists working with children should consider the above mentioned findings and recommendations when elaborating the treatment plan. Moreover, even though based on the differences between study designs, samples and types of exercises among studies, it can difficult to determine a specific type of intervention that would benefit all the children manifesting repetitive behaviors, the studies analyzed in this systematic review include clinically relevant findings that can be used as a base and further adapted to fit different characteristics, needs and capabilities of individuals in future intervention processes.
27
6. References
Abbott, A. E., Linke, A. C., Nair, A., Jahedi, A., Alba, L. A., Keown, C. L., ... & Müller, R. A. (2017). Repetitive behaviors in autism are linked to imbalance of corticostriatal connectivity: a functional connectivity MRI study. Social cognitive and affective
neuroscience, 13(1), 32-42.
American Psychiatric Association (2013). Diagnostic and statistical manual of mental
disorders (DSM-5®). American Psychiatric Pub.
Anderson-Hanley, C., Tureck, K., & Schneiderman, R. L. (2011). Autism and exergaming: effects on repetitive behaviors and cognition. Psychology research and
behavior management, 4, 129.
Autism Spectrum Disorders (2018), retrieved April 1, 2019, from
http://www.nimh.nih.gov/health/publications/autism/complete-index.shtml#pub6
Bahrami, F., Movahedi, A., Marandi, S. M., & Abedi, A. (2012). Kata techniques training consistently decreases stereotypy in children with autism spectrum disorder. Research in
developmental disabilities, 33(4), 1183-1193.
Björck-Åkesson, E. (2019, January). The use of collaborative problem solving. Jönköping University Retrieved from https://pingpong.hj.se/courseId/20341/content.do?id=15921364 [Streamed Lecture]
Bremer, E., Crozier, M., & Lloyd, M. (2016). A systematic review of the behavioural outcomes following exercise interventions for children and youth with autism spectrum disorder. Autism, 20(8), 899-915.
Briggs, J. (2018). Critical Appraisal Tool. Retrieved from http://joannabriggs.org/research/critical-appraisal-tools.html
Bronfenbrenner, U., & Evans, G. W. (2000). Developmental science in the 21st century: Emerging questions, theoretical models, research designs and empirical findings. Social
28
Chan, A. S., Sze, S. L., Siu, N. Y., Lau, E. M., & Cheung, M. C. (2013). A Chinese mind-body exercise improves self-control of children with autism: a randomized controlled trial. PLoS One, 8(7), e68184
Dictionary, M.W. (2004). Merriam-Webster's collegiate dictionary. Merriam-Webster. Accessed February, 2019.
Fournier, K. A., Hass, C. J., Naik, S. K., Lodha, N., & Cauraugh, J. H. (2010). Motor coordination in autism spectrum disorders: a synthesis and meta-analysis. Journal of
autism and developmental disorders, 40(10), 1227-1240.
Jahn, W. T. (2011). The 4 basic ethical principles that apply to forensic activities are respect for autonomy, beneficence, nonmaleficence, and justice. Journal of chiropractic
medicine, 10(3), 225.
Jiménez Martínez, E., Santana Rodríguez, A., Mateos Padorno, C., & Montesdeoca Hernández, R. (2018). Benefits of physical activity for children with autism.
Kern, L., Koegel, R. L., & Dunlap, G. (1984). The influence of vigorous versus mild exercise on autistic stereotyped behaviors. Journal of autism and developmental
disorders, 14(1), 57-67.
Lang, R., Koegel, L. K., Ashbaugh, K., Regester, A., Ence, W., & Smith, W. (2010). Physical exercise and individuals with autism spectrum disorders: A systematic review. Research in Autism Spectrum Disorders, 4(4), 565-576.
Leekam, S. R., Prior, M. R., & Uljarevic, M. (2011). Restricted and repetitive behaviors in autism spectrum disorders: a review of research in the last decade. Psychological
bulletin, 137(4), 562.
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P., ... & Moher, D. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and
elaboration. PLoS medicine, 6(7), e1000100.
Mauro, T. (2018). What It Means When a Child Has Special Needs An Array of Diagnoses and Challenges. Retrieved from
29
Mostert-Kerckhoffs, M. A., Staal, W. G., Houben, R. H., & de Jonge, M. V. (2015). Stop and change: Inhibition and flexibility skills are related to repetitive behavior in children and young adults with autism spectrum disorders. Journal of Autism and Developmental
Disorders, 45(10), 3148-3158.
Neely, L., Rispoli, M., Gerow, S., & Ninci, J. (2015). Effects of antecedent exercise on academic engagement and stereotypy during instruction. Behavior modification, 39(1), 98-116.
Operto, F. F., Martino, F., Rinaldi, A., Cerracchio, A., Salvati, G., Orza, M., ... & Farello, G. (2017). Long-term outcome of autistic spectrum disorder: a retrospective case study in a southern Italian region. Italian journal of pediatrics, 43(1), 83.
Petrus, C., Adamson, S. R., Block, L., Einarson, S. J., Sharifnejad, M., & Harris, S. R. (2008). Effects of exercise interventions on stereotypic behaviours in children with autism spectrum disorder. Physiotherapy Canada, 60(2), 134-145.
Srinivasan, S. M., Park, I. K., Neelly, L. B., & Bhat, A. N. (2015). A comparison of the effects of rhythm and robotic interventions on repetitive behaviors and affective states of children with Autism Spectrum Disorder (ASD). Research in autism spectrum
disorders, 18, 51-63.
Tse, C. A., Pang, C. L., & Lee, P. H. (2018). Choosing an appropriate physical exercise to reduce stereotypic behavior in children with autism spectrum disorders: a non-randomized crossover study. Journal of autism and developmental disorders, 48(5), 1666-1672.
Watt, N., Wetherby, A. M., Barber, A., & Morgan, L. (2008). Repetitive and stereotyped behaviors in children with autism spectrum disorders in the second year of life. Journal of
autism and developmental disorders, 38(8), 1518-1533.
Werling, D. M., & Geschwind, D. H. (2013). Sex differences in autism spectrum disorders. Current opinion in neurology, 26(2), 146.
World Health Organization. (2001). International classification of functioning, disability
